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Published in: Journal of Neurology 11/2018

Open Access 01-11-2018 | Original Communication

StartReact during gait initiation reveals differential control of muscle activation and inhibition in patients with corticospinal degeneration

Authors: Bas J. H. van Lith, Milou J. M. Coppens, Jorik Nonnekes, Bart P. C. van de Warrenburg, Alexander C. Geurts, Vivian Weerdesteyn

Published in: Journal of Neurology | Issue 11/2018

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Abstract

Corticospinal lesions cause impairments in voluntary motor control. Recent findings suggest that some degree of voluntary control may be taken over by a compensatory pathway involving the reticulospinal tract. In humans, evidence for this notion mainly comes from StartReact studies. StartReact is the acceleration of reaction times by a startling acoustic stimulus (SAS) simultaneously presented with the imperative stimulus. As previous StartReact studies mainly focused on isolated single-joint movements, the question remains whether the reticulospinal tract can also be utilized for controlling whole-body movements. To investigate reticulospinal control, we applied the StartReact paradigm during gait initiation in 12 healthy controls and 12 patients with ‘pure’ hereditary spastic paraplegia (HSP; i.e., retrograde axonal degeneration of corticospinal tract). Participants performed three consecutive steps in response to an imperative visual stimulus. In 25% of 16 trials a SAS was applied. We determined reaction times of muscle (de)activation, anticipatory postural adjustments (APA) and steps. Without SAS, we observed an overall delay in HSP patients compared to controls. Administration of the SAS accelerated tibialis anterior and rectus femoris onsets in both groups, but more so in HSP patients, resulting in (near-)normal latencies. Soleus offsets were accelerated in controls, but not in HSP patients. The SAS also accelerated APA and step reaction times in both groups, yet these did not normalize in the HSP patients. The reticulospinal tract is able to play a compensatory role in voluntary control of whole-body movements, but seems to lack the capacity to inhibit task-inappropriate muscle activity in patients with corticospinal lesions.
Literature
1.
go back to reference Baker SN (2011) The primate reticulospinal tract, hand function and functional recovery. J Physiol 589:5603–5612CrossRef Baker SN (2011) The primate reticulospinal tract, hand function and functional recovery. J Physiol 589:5603–5612CrossRef
2.
go back to reference Baker SN, Perez MA (2017) Reticulospinal contributions to gross hand function after human spinal cord injury. J Neurosci 37:9778–9784CrossRef Baker SN, Perez MA (2017) Reticulospinal contributions to gross hand function after human spinal cord injury. J Neurosci 37:9778–9784CrossRef
3.
go back to reference Baker SN, Zaaimi B, Fisher KM, Edgley SA, Soteropoulos DS (2015) Pathways mediating functional recovery. Prog Brain Res 218:389–412CrossRef Baker SN, Zaaimi B, Fisher KM, Edgley SA, Soteropoulos DS (2015) Pathways mediating functional recovery. Prog Brain Res 218:389–412CrossRef
4.
go back to reference Blackstone C, O’Kane CJ, Reid E (2011) Hereditary spastic paraplegias: membrane traffic and the motor pathway. Nat Rev Neurosci 12:31–42CrossRef Blackstone C, O’Kane CJ, Reid E (2011) Hereditary spastic paraplegias: membrane traffic and the motor pathway. Nat Rev Neurosci 12:31–42CrossRef
5.
go back to reference Brown P, Day BL, Rothwell JC, Thompson PD, Marsden CD (1991) The effect of posture on the normal and pathological auditory startle reflex. J Neurol Neurosurg Psychiatry 54:892–897CrossRef Brown P, Day BL, Rothwell JC, Thompson PD, Marsden CD (1991) The effect of posture on the normal and pathological auditory startle reflex. J Neurol Neurosurg Psychiatry 54:892–897CrossRef
6.
go back to reference Carlsen A, Chua R, Inglis JT, Sanderson DJ, Franks IM (2004) Prepared movements are elicited early by startle. J Mot Behav 36:253–264CrossRef Carlsen A, Chua R, Inglis JT, Sanderson DJ, Franks IM (2004) Prepared movements are elicited early by startle. J Mot Behav 36:253–264CrossRef
7.
go back to reference Carlsen AN, Almeida QJ, Franks IM (2012) Startle decreases reaction time to active inhibition. Exp Brain Res 217:7–14CrossRef Carlsen AN, Almeida QJ, Franks IM (2012) Startle decreases reaction time to active inhibition. Exp Brain Res 217:7–14CrossRef
8.
go back to reference Carlsen AN, Dakin CJ, Chua R, Franks IM (2007) Startle produces early response latencies that are distinct from stimulus intensity effects. Exp Brain Res 176:199–205CrossRef Carlsen AN, Dakin CJ, Chua R, Franks IM (2007) Startle produces early response latencies that are distinct from stimulus intensity effects. Exp Brain Res 176:199–205CrossRef
9.
go back to reference Council MR (1981) Aids to the examination of the peripheral nervous system. Her Majesty’s Stationery Office, London, p 1981 Council MR (1981) Aids to the examination of the peripheral nervous system. Her Majesty’s Stationery Office, London, p 1981
10.
go back to reference Crenna P, Frigo C (1991) A motor programme for the initiation of forward-oriented movements in humans. J Physiol 437:635–653CrossRef Crenna P, Frigo C (1991) A motor programme for the initiation of forward-oriented movements in humans. J Physiol 437:635–653CrossRef
11.
go back to reference Engberg I, Lundberg A, Ryall RW (1968) Reticulospinal inhibition of interneurones. J Physiol 194:225–236CrossRef Engberg I, Lundberg A, Ryall RW (1968) Reticulospinal inhibition of interneurones. J Physiol 194:225–236CrossRef
12.
go back to reference Fisher KM, Chinnery PF, Baker SN, Baker MR (2013) Enhanced reticulospinal output in patients with (REEP1) hereditary spastic paraplegia type 31. J Neurol 260:3182–3184CrossRef Fisher KM, Chinnery PF, Baker SN, Baker MR (2013) Enhanced reticulospinal output in patients with (REEP1) hereditary spastic paraplegia type 31. J Neurol 260:3182–3184CrossRef
13.
go back to reference Girolami GL, Shiratori T, Aruin AS (2011) Anticipatory postural adjustments in children with hemiplegia and diplegia. J Electromyogr Kinesiol 21:988–997CrossRef Girolami GL, Shiratori T, Aruin AS (2011) Anticipatory postural adjustments in children with hemiplegia and diplegia. J Electromyogr Kinesiol 21:988–997CrossRef
14.
go back to reference Harding AE (1983) Classification of the hereditary ataxias and paraplegias. Lancet 1:1151–1155CrossRef Harding AE (1983) Classification of the hereditary ataxias and paraplegias. Lancet 1:1151–1155CrossRef
15.
go back to reference Harding AE (1993) Hereditary spastic paraplegias. Semin Neurol 13:333–336CrossRef Harding AE (1993) Hereditary spastic paraplegias. Semin Neurol 13:333–336CrossRef
16.
go back to reference Heckmann CJ, Gorassini MA, Bennett DJ (2005) Persistent inward currents in motoneuron dendrites: implications for motor output. Muscle Nerve 31:135–156CrossRef Heckmann CJ, Gorassini MA, Bennett DJ (2005) Persistent inward currents in motoneuron dendrites: implications for motor output. Muscle Nerve 31:135–156CrossRef
17.
go back to reference Herbert WJ, Powell K, Buford JA (2015) Evidence for a role of the reticulospinal system in recovery of skilled reaching after cortical stroke: initial results from a model of ischemic cortical injury. Exp Brain Res 233:3231–3251CrossRef Herbert WJ, Powell K, Buford JA (2015) Evidence for a role of the reticulospinal system in recovery of skilled reaching after cortical stroke: initial results from a model of ischemic cortical injury. Exp Brain Res 233:3231–3251CrossRef
18.
go back to reference Hermens HJ, Freriks B, Merletti R, Stegeman D, Blok J, Rau G, Disselhorst-Klug C, Hägg G (1999) European recommendations for surface electromyography. Roessingh Res Dev 8:13–54 Hermens HJ, Freriks B, Merletti R, Stegeman D, Blok J, Rau G, Disselhorst-Klug C, Hägg G (1999) European recommendations for surface electromyography. Roessingh Res Dev 8:13–54
19.
go back to reference Honeycutt CF, Kharouta M, Perreault EJ (2013) Evidence for reticulospinal contributions to coordinated finger movements in humans. J Neurophysiol 110:1476–1483CrossRef Honeycutt CF, Kharouta M, Perreault EJ (2013) Evidence for reticulospinal contributions to coordinated finger movements in humans. J Neurophysiol 110:1476–1483CrossRef
20.
go back to reference Honeycutt CF, Perreault EJ (2012) Planning of ballistic movement following stroke: insights from the startle reflex. PLoS One 7:e43097CrossRef Honeycutt CF, Perreault EJ (2012) Planning of ballistic movement following stroke: insights from the startle reflex. PLoS One 7:e43097CrossRef
21.
go back to reference Honeycutt CF, Tresch UA, Perreault EJ (2015) Startling acoustic stimuli can evoke fast hand extension movements in stroke survivors. Clin Neurophysiol 126:160–164CrossRef Honeycutt CF, Tresch UA, Perreault EJ (2015) Startling acoustic stimuli can evoke fast hand extension movements in stroke survivors. Clin Neurophysiol 126:160–164CrossRef
22.
go back to reference Jang SH, Chang CH, Lee J, Kim CS, Seo JP, Yeo SS (2013) Functional role of the corticoreticular pathway in chronic stroke patients. Stroke 44:1099–1104CrossRef Jang SH, Chang CH, Lee J, Kim CS, Seo JP, Yeo SS (2013) Functional role of the corticoreticular pathway in chronic stroke patients. Stroke 44:1099–1104CrossRef
23.
go back to reference Jankowska E, Cabaj A, Pettersson LG (2005) How to enhance ipsilateral actions of pyramidal tract neurons. J Neurosci 25:7401–7405CrossRef Jankowska E, Cabaj A, Pettersson LG (2005) How to enhance ipsilateral actions of pyramidal tract neurons. J Neurosci 25:7401–7405CrossRef
24.
go back to reference Kirkpatrick NJ, Ravichandran VJ, Perreault EJ, Schaefer SY, Honeycutt CF (2018) Evidence for startle as a measurable behavioral indicator of motor learning. PLoS One 13:e0195689CrossRef Kirkpatrick NJ, Ravichandran VJ, Perreault EJ, Schaefer SY, Honeycutt CF (2018) Evidence for startle as a measurable behavioral indicator of motor learning. PLoS One 13:e0195689CrossRef
25.
go back to reference Krishnan V, Kanekar N, Aruin AS (2012) Anticipatory postural adjustments in individuals with multiple sclerosis. Neurosci Lett 506:256–260CrossRef Krishnan V, Kanekar N, Aruin AS (2012) Anticipatory postural adjustments in individuals with multiple sclerosis. Neurosci Lett 506:256–260CrossRef
26.
go back to reference Lang CE, Schieber MH (2003) Differential impairment of individuated finger movements in humans after damage to the motor cortex or the corticospinal tract. J Neurophysiol 90:1160–1170CrossRef Lang CE, Schieber MH (2003) Differential impairment of individuated finger movements in humans after damage to the motor cortex or the corticospinal tract. J Neurophysiol 90:1160–1170CrossRef
27.
go back to reference Lang CE, Schieber MH (2004) Reduced muscle selectivity during individuated finger movements in humans after damage to the motor cortex or corticospinal tract. J Neurophysiol 91:1722–1733CrossRef Lang CE, Schieber MH (2004) Reduced muscle selectivity during individuated finger movements in humans after damage to the motor cortex or corticospinal tract. J Neurophysiol 91:1722–1733CrossRef
28.
go back to reference Lu C, Amundsen Huffmaster SL, Harvey JC, MacKinnon CD (2017) Anticipatory postural adjustment patterns during gait initiation across the adult lifespan. Gait Posture 57:182–187CrossRef Lu C, Amundsen Huffmaster SL, Harvey JC, MacKinnon CD (2017) Anticipatory postural adjustment patterns during gait initiation across the adult lifespan. Gait Posture 57:182–187CrossRef
29.
go back to reference MacKinnon CD, Bissig D, Chiusano J, Miller E, Rudnick L, Jager C, Zhang Y, Mille ML, Rogers MW (2007) Preparation of anticipatory postural adjustments prior to stepping. J Neurophysiol 97:4368–4379CrossRef MacKinnon CD, Bissig D, Chiusano J, Miller E, Rudnick L, Jager C, Zhang Y, Mille ML, Rogers MW (2007) Preparation of anticipatory postural adjustments prior to stepping. J Neurophysiol 97:4368–4379CrossRef
30.
go back to reference Magoun HW, Rhines R (1946) An inhibitory mechanism in the bulbar reticular formation. J Neurophysiol 9:165–171CrossRef Magoun HW, Rhines R (1946) An inhibitory mechanism in the bulbar reticular formation. J Neurophysiol 9:165–171CrossRef
31.
go back to reference Marinovic W, Brauer SG, Hayward KS, Carroll TJ, Riek S (2016) Electric and acoustic stimulation during movement preparation can facilitate movement execution in healthy participants and stroke survivors. Neurosci Lett 618:134–138CrossRef Marinovic W, Brauer SG, Hayward KS, Carroll TJ, Riek S (2016) Electric and acoustic stimulation during movement preparation can facilitate movement execution in healthy participants and stroke survivors. Neurosci Lett 618:134–138CrossRef
32.
go back to reference Marinovic W, de Rugy A, Lipp OV, Tresilian JR (2015) Reply to Maslovat et al. J Neurophysiol 113:3455–3456CrossRef Marinovic W, de Rugy A, Lipp OV, Tresilian JR (2015) Reply to Maslovat et al. J Neurophysiol 113:3455–3456CrossRef
33.
go back to reference Marinovic W, Tresilian JR (2016) Triggering prepared actions by sudden sounds: reassessing the evidence for a single mechanism. Acta Physiol (Oxf) 217:13–32CrossRef Marinovic W, Tresilian JR (2016) Triggering prepared actions by sudden sounds: reassessing the evidence for a single mechanism. Acta Physiol (Oxf) 217:13–32CrossRef
34.
go back to reference Maslovat D, Franks IM, Leguerrier A, Carlsen AN (2015) Responses to startling acoustic stimuli indicate that movement-related activation is constant prior to action: a replication with an alternate interpretation. Physiol Rep 3:e12300CrossRef Maslovat D, Franks IM, Leguerrier A, Carlsen AN (2015) Responses to startling acoustic stimuli indicate that movement-related activation is constant prior to action: a replication with an alternate interpretation. Physiol Rep 3:e12300CrossRef
35.
go back to reference Massion J (1992) Movement, posture and equilibrium: interaction and coordination. Prog Neurobiol 38:35–56CrossRef Massion J (1992) Movement, posture and equilibrium: interaction and coordination. Prog Neurobiol 38:35–56CrossRef
36.
go back to reference McCombe Waller S, Yang CL, Magder L, Yungher D, Gray V, Rogers MW (2016) Impaired motor preparation and execution during standing reach in people with chronic stroke. Neurosci Lett 630:38–44CrossRef McCombe Waller S, Yang CL, Magder L, Yungher D, Gray V, Rogers MW (2016) Impaired motor preparation and execution during standing reach in people with chronic stroke. Neurosci Lett 630:38–44CrossRef
37.
go back to reference McDermott C, White K, Bushby K, Shaw P (2000) Hereditary spastic paraparesis: a review of new developments. J Neurol Neurosurg Psychiatry 69:150–160CrossRef McDermott C, White K, Bushby K, Shaw P (2000) Hereditary spastic paraparesis: a review of new developments. J Neurol Neurosurg Psychiatry 69:150–160CrossRef
38.
go back to reference Nonnekes J, Carpenter MG, Inglis JT, Duysens J, Weerdesteyn V (2015) What startles tell us about control of posture and gait. Neurosci Biobehav Rev 53:131–138CrossRef Nonnekes J, Carpenter MG, Inglis JT, Duysens J, Weerdesteyn V (2015) What startles tell us about control of posture and gait. Neurosci Biobehav Rev 53:131–138CrossRef
39.
go back to reference Nonnekes J, de Niet M, Oude Nijhuis LB, de Bot ST, van de Warrenburg BP, Bloem BR, Geurts AC, Weerdesteyn V (2013) Mechanisms of postural instability in hereditary spastic paraplegia. J Neurol 260:2387–2395CrossRef Nonnekes J, de Niet M, Oude Nijhuis LB, de Bot ST, van de Warrenburg BP, Bloem BR, Geurts AC, Weerdesteyn V (2013) Mechanisms of postural instability in hereditary spastic paraplegia. J Neurol 260:2387–2395CrossRef
40.
go back to reference Nonnekes J, Geurts AC, Nijhuis LB, van Geel K, Snijders AH, Bloem BR, Weerdesteyn V (2014) Reduced StartReact effect and freezing of gait in Parkinson’s disease: two of a kind? J Neurol 261:943–950CrossRef Nonnekes J, Geurts AC, Nijhuis LB, van Geel K, Snijders AH, Bloem BR, Weerdesteyn V (2014) Reduced StartReact effect and freezing of gait in Parkinson’s disease: two of a kind? J Neurol 261:943–950CrossRef
41.
go back to reference Nonnekes J, Oude Nijhuis LB, de Niet M, de Bot ST, Pasman JW, van de Warrenburg BP, Bloem BR, Weerdesteyn V, Geurts AC (2014) StartReact restores reaction time in HSP: evidence for subcortical release of a motor program. J Neurosci 34:275–281CrossRef Nonnekes J, Oude Nijhuis LB, de Niet M, de Bot ST, Pasman JW, van de Warrenburg BP, Bloem BR, Weerdesteyn V, Geurts AC (2014) StartReact restores reaction time in HSP: evidence for subcortical release of a motor program. J Neurosci 34:275–281CrossRef
42.
go back to reference Nonnekes J, Scotti A, Oude Nijhuis LB, Smulders K, Queralt A, Geurts AC, Bloem BR, Weerdesteyn V (2013) Are postural responses to backward and forward perturbations processed by different neural circuits? Neuroscience 245:109–120CrossRef Nonnekes J, Scotti A, Oude Nijhuis LB, Smulders K, Queralt A, Geurts AC, Bloem BR, Weerdesteyn V (2013) Are postural responses to backward and forward perturbations processed by different neural circuits? Neuroscience 245:109–120CrossRef
43.
go back to reference Nonnekes J, van Lith B, van de Warrenburg BP, Weerdesteyn V, Geurts ACH (2017) Pathophysiology, diagnostic work-up and management of balance impairments and falls in patients with hereditary spastic paraplegia. J Rehabil Med 49:369–377CrossRef Nonnekes J, van Lith B, van de Warrenburg BP, Weerdesteyn V, Geurts ACH (2017) Pathophysiology, diagnostic work-up and management of balance impairments and falls in patients with hereditary spastic paraplegia. J Rehabil Med 49:369–377CrossRef
44.
go back to reference Owen M, Ingo C, Dewald JPA (2017) Upper extremity motor impairments and microstructural changes in bulbospinal pathways in chronic hemiparetic stroke. Front Neurol 8:257CrossRef Owen M, Ingo C, Dewald JPA (2017) Upper extremity motor impairments and microstructural changes in bulbospinal pathways in chronic hemiparetic stroke. Front Neurol 8:257CrossRef
45.
go back to reference Pestronk A, Florence J, Levine T, Al-Lozi MT, Lopate G, Miller T, Ramneantu I, Waheed W, Stambuk M (2004) Sensory exam with a quantitative tuning fork: rapid, sensitive and predictive of SNAP amplitude. Neurology 62:461–464CrossRef Pestronk A, Florence J, Levine T, Al-Lozi MT, Lopate G, Miller T, Ramneantu I, Waheed W, Stambuk M (2004) Sensory exam with a quantitative tuning fork: rapid, sensitive and predictive of SNAP amplitude. Neurology 62:461–464CrossRef
46.
go back to reference Peterson BW, Maunz RA, Pitts NG, Mackel RG (1975) Patterns of projection and braching of reticulospinal neurons. Exp Brain Res 23:333–351CrossRef Peterson BW, Maunz RA, Pitts NG, Mackel RG (1975) Patterns of projection and braching of reticulospinal neurons. Exp Brain Res 23:333–351CrossRef
47.
go back to reference Peterson BW, Pitts NG, Fukushima K (1979) Reticulospinal connections with limb and axial motoneurons. Exp Brain Res 36:1–20CrossRef Peterson BW, Pitts NG, Fukushima K (1979) Reticulospinal connections with limb and axial motoneurons. Exp Brain Res 36:1–20CrossRef
48.
go back to reference Queralt A, Valls-Sole J, Castellote JM (2010) Speeding up gait initiation and gait-pattern with a startling stimulus. Gait Posture 31:185–190CrossRef Queralt A, Valls-Sole J, Castellote JM (2010) Speeding up gait initiation and gait-pattern with a startling stimulus. Gait Posture 31:185–190CrossRef
49.
go back to reference Rajachandrakumar R, Fraser JE, Schinkel-Ivy A, Inness EL, Biasin L, Brunton K, McIlroy WE, Mansfield A (2017) Atypical anticipatory postural adjustments during gait initiation among individuals with sub-acute stroke. Gait Posture 52:325–331CrossRef Rajachandrakumar R, Fraser JE, Schinkel-Ivy A, Inness EL, Biasin L, Brunton K, McIlroy WE, Mansfield A (2017) Atypical anticipatory postural adjustments during gait initiation among individuals with sub-acute stroke. Gait Posture 52:325–331CrossRef
50.
go back to reference Rothwell JC (2006) The startle reflex, voluntary movement, and the reticulospinal tract. Suppl Clin Neurophysiol 58:223–231CrossRef Rothwell JC (2006) The startle reflex, voluntary movement, and the reticulospinal tract. Suppl Clin Neurophysiol 58:223–231CrossRef
51.
go back to reference Salinas S, Proukakis C, Crosby A, Warner TT (2008) Hereditary spastic paraplegia: clinical features and pathogenetic mechanisms. Lancet Neurol 7:1127–1138CrossRef Salinas S, Proukakis C, Crosby A, Warner TT (2008) Hereditary spastic paraplegia: clinical features and pathogenetic mechanisms. Lancet Neurol 7:1127–1138CrossRef
52.
go back to reference Sousa AS, Silva A, Santos R (2015) Ankle anticipatory postural adjustments during gait initiation in healthy and post-stroke subjects. Clin Biomech (Bristol Avon) 30:960–965CrossRef Sousa AS, Silva A, Santos R (2015) Ankle anticipatory postural adjustments during gait initiation in healthy and post-stroke subjects. Clin Biomech (Bristol Avon) 30:960–965CrossRef
53.
go back to reference Trompetto C, Marinelli L, Mori L, Pelosin E, Curra A, Molfetta L, Abbruzzese G (2014) Pathophysiology of spasticity: implications for neurorehabilitation. Biomed Res Int 2014:354906CrossRef Trompetto C, Marinelli L, Mori L, Pelosin E, Curra A, Molfetta L, Abbruzzese G (2014) Pathophysiology of spasticity: implications for neurorehabilitation. Biomed Res Int 2014:354906CrossRef
54.
go back to reference Valls-Sole J, Rothwell JC, Goulart F, Cossu G, Munoz E (1999) Patterned ballistic movements triggered by a startle in healthy humans. J Physiol 516(Pt 3):931–938CrossRef Valls-Sole J, Rothwell JC, Goulart F, Cossu G, Munoz E (1999) Patterned ballistic movements triggered by a startle in healthy humans. J Physiol 516(Pt 3):931–938CrossRef
55.
go back to reference Zaaimi B, Edgley SA, Soteropoulos DS, Baker SN (2012) Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkey. Brain 135:2277–2289CrossRef Zaaimi B, Edgley SA, Soteropoulos DS, Baker SN (2012) Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkey. Brain 135:2277–2289CrossRef
Metadata
Title
StartReact during gait initiation reveals differential control of muscle activation and inhibition in patients with corticospinal degeneration
Authors
Bas J. H. van Lith
Milou J. M. Coppens
Jorik Nonnekes
Bart P. C. van de Warrenburg
Alexander C. Geurts
Vivian Weerdesteyn
Publication date
01-11-2018
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 11/2018
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-018-9027-0

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